Antimicrobial Usage in Smallholder Poultry Production in Nigeria

The indiscriminate use of antimicrobials in livestock production is of increasing concern due to the threat of antimicrobial resistance in both humans and animals. Much emphasis has been placed on intensively managed poultry production systems, which routinely use antimicrobials as against smallholder poultry production systems (SPPS). Therefore, this study investigated the use of antimicrobials among smallholder poultry farmers in Nigeria, and compared the prevalence of antimicrobial drug use against the practice of ethnoveterinary medicine (EVM). A cross-sectional study was conducted in five states (agroecologies) of Nigeria using structured questionnaires administered on a total of 350 farmers. The practice of EVM was prevalent among most of the farmers (39%). The western method (pharmaceuticals) was practiced by a large proportion of farmers (60%), either solely (25%) or in combination with EVM (35%). Antimicrobials were used primarily for treatment and prevention of diseases (78%). Semi-scavenging system of production had the highest proportion (49%) of farmers using antimicrobials, compared to semi-intensive (37%) and scavenging (14%) systems. Gender (χ2 = 9.30, p = 0.01), and location (χ2 = 216.86, p ≤ 0.001), influenced farmers' choice of methods for bird treatment. Education (odds ratio [OR] odds ratio [OR] 3.06, 95% CI 2.10–4.44), income (OR 1.99, 95% CI 1.10–3.59) and management system (OR 1.97, CI% 1.1–3.45) were most associated with antimicrobial use. Critically important antibiotics, with lower to higher risk of antimicrobial resistance, were used by farmers (40%). These findings showed the indiscriminate use of antimicrobials by farmers and the potential risk of antimicrobial resistance within the SPPS in Nigeria.


Introduction
e use of antimicrobials in livestock production, for disease prevention and growth promotion, is of increasing concern owing to the threat of antimicrobial resistance in both humans and animals [1]. Antimicrobial resistance has been described as one of the biggest threats to humanity, affecting critical areas such as global health, food security and livelihoods [2,3]. Overdependence on antimicrobials by farmers, and their indiscriminate and inappropriate use are the primary divers of antimicrobial resistance [4][5][6]. Livestock production under intensive management system is characterized by routine use of antimicrobials, and has been associated with increased antimicrobial resistance, especially in poultry [7]. On the other hand, the use of antimicrobials in scavenging and semi-scavenging production systems of smallholder poultry is generally considered low due to the practice of ethnoveterinary medicine by resource-poor farmers [8,9]. However, recent studies have observed the increasing use of antimicrobials within the free-range, village or backyard poultry system [4,10].
Also, the introduction of improved chicken breeds into smallholder poultry production systems (SPPS) as an intervention for increasing food security and livelihoods among rural households in sub-Saharan Africa [11][12][13] has highlighted the associated high risk of mortality in the flock due to the heterogenous condition of such environments for diseases and infection [14,15]. In order to prevent this risk, and increase the survivability of the improved chickens, smallholder poultry farmers are exposed to the use of antimicrobials as against adopting improved biosafety and biosecurity measures in reducing the high disease burden within the production environment [10,16]. Unavailability of veterinarians and animal health workers in rural communities is a contributory factor predisposing smallholder poultry farmers to indiscriminate use of antimicrobials [1,16]. e improved, tropically adapted chicken breeds (FUNAAB Alpha, Noiler, Kuroiler, Sasso, ShikaBrown) were introduced to smallholder poultry farmers in Nigeria through the African Chicken Genetic Gains project (2015-2019) [11,17]. ese breeds, coupled with the existing local chicken ecotypes are a major source of animal protein (eggs, meat) in the country since smallholder poultry contribute 65-77% of the total chicken production in Nigeria [18]. is huge food resource also presents a potential risk and challenge to food safety due to the abuse of antimicrobials within the production systems. erefore, the objective of this study was to investigate the use of antimicrobials among smallholder poultry farmers in Nigeria, as well as the prevalence of such use in relation to ethnoveterinary practices within the SPPS.

Materials and Methods
is study (cross-sectional) was conducted in five states (Rivers, Imo, Kwara, Nasarawa, Kebbi) of Nigeria each representing different agroecologies. e agroecological features of these states have been described by Yakubu et al. [19], and Bamidele and Amole [18]. A total of 350 (70 per state) smallholder poultry farmers participated in the study. e sampling method and inclusion criteria were as described by [18]. All the farmers provided informed consent and the study was approved by the Review Committee of the CGIAR COVID-19 Hub: ILRI Nigeria 2021.
Structured questionnaires were designed to provide information in the following areas: socio-demography, poultry production, disease and health management, and training in animal health. Specifically, the questionnaires elicited information on the knowledge of antimicrobial resistance, perceptions on the risks and implications of antimicrobial use, attitude of farmers towards antimicrobial usage, and the impact of COVID-19 pandemic on the procurement of antimicrobials for animal use. e questionnaires were administered to the farmers at their respective homes by trained field officers, using Google Forms accessed on smartphones. e data collection spanned 14 days (14-28 September, 2021). Data were analysed using descriptive and inferential statistics in IBM-SPSS (version 20). Data visualisations were presented using PAST (version 4.03) and Microsoft Excel (Office 2019). e antimicrobial drugs were classified based on their active ingredients and class [20], AWaRe (Access, Watch, Reserve) group list of antimicrobials [21], and WHO categorisation of importance of antibiotics in human medicine [22]. e official Central Bank of Nigeria's average monthly exchange rate used in the study was NGN 410.7 to 1 USD [23].

Treatment Methods Used by Farmers.
e treatment options adopted by farmers for treating their flock were traditional/ethnoveterinary method (39.4%), western method (i.e. use of pharmaceuticals) (25.1%), and a combination of both traditional and western methods (35.4%) ( Table 4). Rivers and Kwara states accounted for about onethird (62.3%) of the farmers who only used traditional/ ethnoveterinary method while Kebbi accounted for over two-thirds (68.2%) of the farmers who used western method. Imo and Nasarawa states had the highest percentage of farmers (32.3%) who used both traditional and western methods. A vast majority of the farmers in Kebbi (92.9%), Imo (74.3%), and Nasarawa (58.6%) states used pharmaceuticals, either alone or in combination with ethnoveterinary medicines. Gender (χ 2 � 9.30, p � 0.01), location (χ 2 � 216.86, p ≤ 0.01), breed-type (χ 2 � 155.92, p ≤ 0.01) and management system (χ 2 � 25.08, p ≤ 0.01) were significantly associated with the methods of disease treatment used by farmers. More female farmers (43.8%) used the traditional method than the other methods (Western: 21.3%, Both Western and Traditional: 34.9%). Most of the male farmers (36.6%) used both traditional and western methods as against either the traditional (28.7%) or western (34.7%) e primary reason for using the traditional method by most farmers in Nasarawa (34.5%), Rivers (43.2%) and Kwara (40.5%) states was affordability. Most farmers in both Kebbi (100%) and Imo (61.1%) states indicated the ease of availability and accessibility as their primary reason. Most of the farmers identified affordability and availability/accessibility of ethnoveterinary medicines as the primary (38.4%) and secondary (42.8%) reasons for the use of the traditional method.

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Over half (54.3%) of the farmers completed the required dosage during treatment compared to those (29.7%) who did not complete the dosage. Kebbi (50.0%) and Imo (46.0%) states accounted for most (98.4%) of the farmers who do not complete the required treatment dosage. Over one-tenth (16.0%) of the farmers did not know there was a required dosage for antimicrobials usage. A vast majority (87.3%) of the farmers stored the drugs somewhere in the house, with only a few (7.6%) using refrigerator. About one-third (31.6%) of the farmers knew the names of the antimicrobials administered. Most of the farmers (45.8%) did not know the names of the antimicrobials given to the birds but about onefourth (22.6%) of these farmers could describe the antimicrobials. Figure 1 shows the antimicrobial drugs commonly used by the farmers. All the antimicrobials, except oxytetracycline (watch list) were on the access group list of antimicrobials [20]. Tetracycline was the most commonly    Table 6 highlights the influence of the independent factors (location, gender, education, age, income, farming experience, and management system) in predicting antimicrobial usage. e model shows that the factors were good predictors (β = 0.429, df = 1, p < 0.05) of antimicrobials use among the farmers. Educational level, family income, management system, age, location, and breed-type were 3.055, 1.987, 1.965, 0.741, 0.510, and 0.398 times more likely (p < 0.05) to influence farmers' use of antimicrobials, respectively. Gender, and farmers' years of keeping chicken did not have a statistically significant effect (p > 0.05) on the use of antimicrobials.

Discussion
Globally, the indiscriminate use of antibiotics in poultry production is a driver of antimicrobial resistance within the food chain. Antimicrobial use in smallholder poultry production in Nigeria is of particular importance due to the increasing shift in consumer preference for organicallyraised village chickens (local, improved) produced under scavenging and semi-scavenging production systems. Chickens reared under such systems have been reported to have a lower risk of antimicrobial resistance [23,24] because women who are the primary keepers of these birds, also serve as custodians of the indigenous veterinary knowledge (ethnoveterinary medicine) used in the treatment of diseases and general flock management [8,10,25,26]. e result of this study agrees with previous studies on the role and dominance of women in smallholder poultry production in developing countries [26][27][28]. Compared to men (10.9%), over one-third (37.4%) of the women (37.4%) sampled in this study were uneducated (0 years of schooling). e high illiteracy observed among women limits the technical efficiency, productivity and performance of the primary chicken producers within the smallholder poultry value chain [29][30][31]. Specifically, it limits the capacity to adequately administer, monitor and keep records of antimicrobial use on the farm. is is supported by our findings on the record keeping, handling, storage and administration of antimicrobials by farmers sampled in this study.

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High illiteracy among women also suggests that the women are innumerate. is portends a high possibility for the indiscriminate use of antimicrobials by resource-poor women, majority (70.3%) of whom earned below NGN 30,000 per month (i.e. USD 2.4/person/day). is is consistent with the overall poor outlook of women incomes and lower wages compared to men in smallholder farming [32]. Also, in a recent study, Bamidele and Amole [18] reported lower monthly incomes for women chicken producers in Nigeria compared to men.
Over half (54.0%) of the farmers had between 0 and 10 years' experience keeping smallholder poultry. is is similar to the number of years of farming experience reported by Alemayehu et al. [33], but is at variance with the report by Xu et al. [34] who observed that most farmers in Northwestern China had between 10 and 19 years farming experience. Despite the high percentage of farmers (83.1%) with over 5 years farming experience, a large proportion (88.9%) of the farmers had never been trained on poultry keeping, and only a few (11.1%) had received a form of training on animal health. Lack of basic training in husbandry and health management is a characteristic description of smallholder farming systems because farmers' access to quality training by subject-matter specialists and agricultural extension agents is poor and limited in rural communities [34,35]. Keeping of improved and exotic chickens under the semi-scavenging and semi-intensive systems of production requires farmers to be adequately trained and informed on the management (housing, nutrition, health, biosecurity) skills applicable under such production systems [31]. Most farmers (39.4%) in this study, especially women practiced ethnoveterinary medicine (traditional method) for disease treatment and health management.
is was most common with farmers who only kept local chickens (53.6%) as against those who reared exotic (42.0%) and improved (4.4%) chickens in addition to the local chicken ecotypes. Compared with the scavenging (16.0%) and semi-intensive (30.4%) production systems, the semi-scavenging system of production had the highest percentage (53.6%) of farmers applying the indigenous veterinary knowledge for bird treatment. Affordability (low cost) (38.4%) and availability (42.8%) were identified as the highest primary and secondary factors influencing the use of ethnoveterinary medicine, respectively. Previous studies have equally identified accessibility and low cost as the main drivers of ethnoveterinary medicine among farmers in SPPS [26,36,37]. Unsurprisingly, animal welfare, food safety and environmental considerations were the least factors motivating the use of traditional and local medicines on smallholder poultry farms.
Over two-thirds (35.4%) of the farmers were observed to be using a combination of ethnoveterinary and western methods of treatment in disease treatment and health management.
is practice was common with farmers keeping exotic chickens (50.8%) in addition to local chickens than with those who kept improved (33.1%) breeds. It was least common with farmers who only kept local chickens (16.1%). While low cost of ethnoveterinary medicine was a major driver for its application, farmers who solely used western methods of pharmaceuticals treatment or in combination with traditional local herbs, indicated the cost implication of antimicrobial administration on the overall production and profitability of the farm enterprise. However, it has been reported that the cost of antimicrobials is relatively low and its use does not affect the profitability and economics of production in smallholdings [38,39]. Administration of the antimicrobial drugs was mostly through water, a route previously reported as being the most used by poultry farmers [40][41][42].
is study observed a strong association between the locations (agroecology) and the various factors (primary and secondary) influencing the use of antimicrobials by farmers. ese findings are in consonance with the reported intricate linkage between farmers' use of antimicrobials and veterinarians, poultry dealers and merchants, and sales representatives of feed companies and pharmaceuticals [43]. Our findings show that the behavioural tendency of farmers towards using antimicrobials is driven by the onset of any sign of illness in the birds, even though most of the farmers have not received any formal training on the identification of diseases and animal health management.
is behaviour may explain the observed high percentage of farmers who indulge in self-prescription based on self-diagnosis, consequently risking an incorrect diagnosis and wrong use of antimicrobial drugs [44].
As previously reported by other studies for both commercial poultry (intensive) and small-scale poultry [32,[43][44][45], our findings also show multiple antimicrobial Veterinary Medicine International drug usage in SPPS. Multi-drug use was most common in semi-intensive production systems (69.7%) than in the other two systems (scavenging: 6.1%, Semi-scavenging: 24.2%), and was common with farmers who kept exotic (53.0%) and improved (33.3%) breeds. e high prevalence of multi-drug use observed in this study is similar to that previously reported for commercial and intensively managed farms in both developed and developing countries [32,41,46]. Unlike in developed nations, where policies have been enacted to prevent indiscriminate use of antimicrobials in livestock production, the ease of purchasing over-the-counter antimicrobial drugs, lack of training, and poor regulation of veterinary and animal practices are some of the factors fueling multi-drug use in the developing countries [6,47].
Tetracycline in combination with either Flagyl ® (24.2%) or Ampiclox ® (18.2%) were the most predominant multi-drug used by farmers in this study. Tetracycline is reportedly one of the most commonly used antibiotics drug class in Africa [40,43,48]. All the antimicrobials were on the access list of antibiotic drug groups, except oxytetracyline, which was on the watch list. According to WHO [21], antibiotics on the access and watch lists have lower and higher resistance potentials than those on the reserve list (highest potential), respectively. is study identified the presence of the critically important (4 classes), highly important (5 classes), and important (1 class) antibiotic drugs used in human medicine [22]. e critically important antibiotic drugs were used by a larger proportion of the farmers (40%), than the other two classes. e presence of critically important antibiotics, with lower to higher resistance potential presents a potential public health threat, of antimicrobial resistance, to Nigerians who are increasingly demanding for organically-raised village chickens in place of the intensively-produced poultry products [49][50][51]. Our finding is consistent with the ranking of antimicrobial drug categorisation in Bangladesh, a country with similar economic and agricultural status as Nigeria [45]. e knowledge and awareness of farmers on the conditions (shelf-life, storage, withdrawal period, drug residue) for antimicrobial usage and the associated risks to humans, animals and the environment was poor. In addition to age and educational level, location, as a description of the agroecological zones was a significant predictor of antimicrobial usage among smallholder poultry farmers in Nigeria.

Conclusion
To the best of our knowledge, this study is the first to report on antimicrobial usage in SPPS across major agroecological zones of Nigeria. Most farmers still practice ethnoveterinary medicine. Antimicrobial drugs were used by farmers who kept both improved (FUNAAB Alpha, Noiler, Sasso, Kuroiler, ShikaBrown) and exotic (Broiler and layers) birds in addition to the local chicken ecotypes. Education, income and management system had the highest of influence on antimicrobial use. Multi-drug use was prevalent in the semiintensive system of production with tetracycline being the drug mostly administered in combination with Flagyl ® or Ampiclox ® . ere is a high risk of indiscriminate use of antimicrobial drugs within SPPS in Nigeria because of the high level of illiteracy observed among the women, who are the primary producers of village chickens. e use of critically important antibiotics threatens the consumption of poultry products, and presents smallholder poultry as a reservoir for antimicrobial resistance in humans. Provision of specialized trainings on animal disease and health management among smallholder poultry farmers will improve farmers' knowledge and awareness of antimicrobial resistance and stem the tide of antimicrobial drug abuse in livestock production.

Data Availability
Data are available on request from the corresponding author. After institutional review, all data will be publicly available on the ILRI dataset portal at https://data.ilri.org/ portal/.

Conflicts of Interest
e authors declare there are no conflicts of interest regarding the publication of this paper.